Structural and thermal stability analysis of Escherichia coli and Alicyclobacillus acidocaldarius thioredoxin revealed a molten globule-like state in thermal denaturation pathway of the proteins: an infrared spectroscopic study
Structural and thermal stability analysis of Escherichia coli and Alicyclobacillus acidocaldarius thioredoxin revealed a molten globule-like state in thermal denaturation pathway of the proteins: an infrared spectroscopic study(537 views) Pedone E, Bartolucci S, Rossi M, Pierfederici FM, Scire A, Cacciamani T, Tanfani F
Keywords: Fourier-Transform Ir (ftir) Spectroscopy, Molten Globule-Like State, Protein Aggregation, Thermostability, Thioredoxin, Two-Dimensional Ir Correlation Analysis, Escherichia Coli, Fourier Transform Infrared Spectroscopy, Molecular Structure, Thermodynamic Stability, Mutants, Biochemistry, Bacterial Protein, Alicyclobacillus Acidocaldarius, Analytic Method, Article, Controlled Study, Nonhuman, Priority Journal, Protein Structure, Temperature Dependence, Enzyme Stability, Protein Conformation, Protein Denaturation, Spectrophotometry, Bacteria (microorganisms),
Affiliations: *** IBB - CNR ***
Ist. di Biostrutture e Bioimmagini, C.N.R., Via Mezzocannone 6, 80134, Napoli, Italy
Dipartimento di Chimica Biologica, Univ. Studi di Napoli Federico II, via Mezzocannone 16, 80134 Napoli, Italy
Ist. di Biochimica delle Proteine, via P. Castellino 111, 80131 Napoli, Italy
Dipartimento di Scienze Chimiche, Univ. degli Studi di Catania, viale A. Doria 6, 95125 Catania, Italy
Istituto di Biochimica, Univ. Politecnica delle Marche, via Ranieri, 60131 Ancona, Italy
References: Eklund, H., Gleason, F.K., Holmgren, A., Structural and functional relations among thioredoxins of different species (1991) Proteins: Struct., Funct., Genet., 11, pp. 13-2
Buchanan, B.B., Schurmann, P., Decottignies, P., Lozano, R.M., Thioredoxin: A multifunctional regulatory protein with a bright future in technology and medicine (1994) Arch Biochem. Biophys., 314, pp. 257-260
LaVallie, E.R., Di Blasio, E.A., Kovacic, S., Grant, K.L., Schendel, P.F., McCoy, J.M., A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. coli cytoplasm (1993) Bio/Technology, 11, pp. 187-193
Yasukawa, T., Kanei-Ishii, C., Maekawa, T., Fujimoto, J., Yamamoto, T., Ishii, S., Increase of solubility of foreign proteins in Escherichia coli by coproduction of the bacterial thioredoxin (1995) J. Biol. Chem., 270, pp. 25328-25331
Bartolucci, S., Guagliardi, A., Pedone, E., De Pascale, D., Cannio, R., Camardella, L., Rossi, M., Facci, P., Thioredoxin from Bacillus acidocaldarius: Characterization, high-level expression in Escherichia coli and molecular modelling (1997) Biochem J., 328, pp. 277-285
Pedone, E., Bartolucci, S., Rossi, M., Saviano, M., Computational analysis of the thermal stability in thioredoxins: A molecular dynamics approach (1998) J. Biomol. Struct. Dyn., 16, pp. 437-446
Pedone, E., Cannio, R., Saviano, M., Rossi, M., Bartolucci, S., Prediction and experimental testing of Bacillus acidocaldarius thioredoxin stability (1999) Biochem. J., 15, pp. 309-317
Pedone, E., Saviano, M., Rossi, M., Bartolucci, S., A single point mutation (Glu85Arg) increases the stability of the thioredoxin from Escherichia coli (2001) Protein Eng., 14, pp. 255-260
Ladbury, J.E., Wynn, R., Homme, W., Hellinga, H.W., Julian, M., Sturtevant, J.M., Stability of oxidized Eseherichia coli thioredoxin and its dependence on protonation of the aspartic acid residue in the 26 position (1993) Biochemistry, 32, pp. 7526-7530
Maier, C.S., Schimerlik, M.I., Deinzer, M.L., Thermal denaturation of Escherichia coli thioredoxin studied by hydrogen/deuterium exchange and electrospray ionization masis spectrometry: Monitoring a two-state protein unfolding transition (1999) Biochemistry, 38, pp. 1136-1143
Salomaa, P., Schaleger, L.L., Long, F.A., Solvent deuterium isotope effects on acid-base equilibria (1964) J. Am. Chem. Soc., 88, pp. 1-7
Paolini, S., Tanfani, F., Fini, C., Bertoli, E., Pelosi, P., Porcine odorant-binding protein: Structural stability and ligand affinities measured by Fourier transform infrared spectroscopy and fluorescence spectroscopy (1999) Biochim. Biophys. Acta, 1431, pp. 179-188
Noda, I., Generalized two-dimensional correlation method applicable to infrared, raman and other types of spectroscopy (1993) Appl. Spectrosc., 47, pp. 1329-1336
Sasic, S., Muszynski, A., Ozaki, Y., A new possibility of the generalized two-dimensional correlation spectroscopy. 1. Sample-sample correlation spectroscopy (2000) J. Phys Chem. A, 104, pp. 6380-6387
Fabian, H., Mantsch, H.H., Schultz, C.P., Two-dimensional IR correlation spectroscopy: Sequential events in the unfolding process of the λ Cro-V55C repressor protein (1999) Proc Natl. Acad. Sci. U.S.A., 96, pp. 13153-13158
Osborne, H.B., Nabedryk-Viala, E., Infrared measurements of peptide hydrogen exchange in rhodopsin (1982) Methods Enzymol., 88, pp. 676-680
Byler, D.M., Susi, H., Examination of the secondary structure of proteins by deconvolved FTIR spectra (1986) Biopolymers, 25, pp. 469-487
Arrondo, J.L.R., Muga, A., Castresana, J., Goñi, F.M., Quantitative studies of the structure of proteins in solutions by Fourier-transform infrared spectroscopy (1993) Prog. Biophys. Mol. Biol., 59, pp. 23-56
Surewicz, W.K., Mantsch, H.H., Chapman, D., Determination of protein secondary structure by Fourier transform infrared spectroscopy: A critical assessment (1993) Biochemistry, 32, pp. 389-394
Casal, H.L., Kohler, U., Mantsch, H.H., Structural and conformational changes of β-lactoglobulin B: An infrared spectroscopic study of the effect of pH and temperature (1988) Biochim. Biophys. Acta, 957, pp. 11-20
Jackson, M., Mantsch, H.H., Halogenated alcohols as solvent for proteins: FTIR spectroscopic studies (1992) Biochim. Biophys. Acta, 1118, pp. 139-143
Nicastro, G., De Chiara, C., Pedone, E., Tatò, M., Rossi, M., Bartolucci, S., NMR solution structure of a novel thioredoxin from Bacillus acidocaldarius. Possible determinants of protein stability (2000) Eur. J. Biochem., 267, pp. 403-413
Krimm, S., Bandekar, J., Vibrational spectroscopy and conformation of peptides, polypeptides and proteins (1986) Adv. Protein Chem., 38, pp. 181-364
Chirgadze, Y.N., Fedorow, O.W., Trushina, N.P., Estimation of amino acid residue side-chain absorption in the infrared spectra of protein solutions in heavy water (1975) Biopolymers, 14, pp. 679-694
Banecki, B., Zylicz, M., Bertoli, E., Tanfani, F., Structural and functional relationships in Dnak and Dnak756 heat-shock proteins from E. coli (1992) J. Biol. Chem., 267, pp. 25051-25058
Leonard, M., Maentele, W., Fourier transform infrared spectroscopy and electrochemistry of the primary electron donor in Rhodobacter sphaeroides and Rhodopseudomonas viridis reaction center: Vibrational modes of the pigments in situ and evidence for protein and water modes affected by P* formation (1993) Biochemistry, 32, pp. 4532-4538
Ptitsyn, O.B., The molten globule state (1992) Protein Folding, pp. 243-300. , Creighton, T. E., ed. W. H. Freeman and Company, New York
Filosa, A., Wang, Y., Ismail, A.A., Englich, A.M., Two-domensional infrared correlation spectroscopy as a probe of sequential events in the thermal unfolding of cytochromes c (2001) Biochemistry, 40, pp. 8256-8263
Martin, J.L., Thioredoxin: A fold for all reasons (1995) Structure, 3, pp. 245-250. , Cambridge, MA, U.S.A
Kennedy, D.F., Crisma, M., Toniolo, C., Capman, D., Studies of peptides forming 310- and α-helices and β-bend ribbon structures in organic solutions and in model biomembranes by Furier transform infrared spectroscopy (1991) Biochemistry, 30, pp. 6541-6548
Soto, C., Protein misfolding and disease
protein refolding and therapy (2001) FEBS Lett., 498, pp. 204-207
Bychkova, V.E., Dujsekina, A.E., Klenin, S.I., Tiktopulo, E.I., Uversky, V.N., Ptitsyn, O.B., Molten globule-like state of cytochrome c under conditions simulating those near the membrane surface (1996) Biochemistry, 35, pp. 6058-6063
Bychkova, V.E., Pain, R.H., Ptitsyn, O.B., The molten globule state is involved in the translocation of proteins across membranes? (1988) FEBS Lett., 238, pp. 231-234
Dolgikh, D.A., Gilmanshin, R.I., Brazhnikov, E.V., Bychkova, V.E., Semisotnov, G.V., Venyaminov, S.Yu., Ptitsyn, O.B., α-lactalbumin: Compact state with fluctuating tertiary structure? (1981) FEBS Lett., 138, pp. 311-315
Dolgikh, D.A., Abaturov, L.V., Bolotina, I.A., Brazhnikov, E.V., Bushuev, V.N., Bychkova, V.E., Gilmanshin, R.I., Ptitsyn, O.B., Compact state of a protein molecule with pronounced small-scale mobility: Bovine α-lactalbumin (1985) Eur. Biophys. J., 13, pp. 109-121
Buchanan, B. B., Schurmann, P., Decottignies, P., Lozano, R. M., Thioredoxin: A multifunctional regulatory protein with a bright future in technology and medicine (1994) Arch Biochem. Biophys., 314, pp. 257-260
LaVallie, E. R., Di Blasio, E. A., Kovacic, S., Grant, K. L., Schendel, P. F., McCoy, J. M., A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. coli cytoplasm (1993) Bio/Technology, 11, pp. 187-193
Ladbury, J. E., Wynn, R., Homme, W., Hellinga, H. W., Julian, M., Sturtevant, J. M., Stability of oxidized Eseherichia coli thioredoxin and its dependence on protonation of the aspartic acid residue in the 26 position (1993) Biochemistry, 32, pp. 7526-7530
Maier, C. S., Schimerlik, M. I., Deinzer, M. L., Thermal denaturation of Escherichia coli thioredoxin studied by hydrogen/deuterium exchange and electrospray ionization masis spectrometry: Monitoring a two-state protein unfolding transition (1999) Biochemistry, 38, pp. 1136-1143
Osborne, H. B., Nabedryk-Viala, E., Infrared measurements of peptide hydrogen exchange in rhodopsin (1982) Methods Enzymol., 88, pp. 676-680
Byler, D. M., Susi, H., Examination of the secondary structure of proteins by deconvolved FTIR spectra (1986) Biopolymers, 25, pp. 469-487
Arrondo, J. L. R., Muga, A., Castresana, J., Go i, F. M., Quantitative studies of the structure of proteins in solutions by Fourier-transform infrared spectroscopy (1993) Prog. Biophys. Mol. Biol., 59, pp. 23-56
Surewicz, W. K., Mantsch, H. H., Chapman, D., Determination of protein secondary structure by Fourier transform infrared spectroscopy: A critical assessment (1993) Biochemistry, 32, pp. 389-394
Casal, H. L., Kohler, U., Mantsch, H. H., Structural and conformational changes of -lactoglobulin B: An infrared spectroscopic study of the effect of pH and temperature (1988) Biochim. Biophys. Acta, 957, pp. 11-20
Chirgadze, Y. N., Fedorow, O. W., Trushina, N. P., Estimation of amino acid residue side-chain absorption in the infrared spectra of protein solutions in heavy water (1975) Biopolymers, 14, pp. 679-694
Ptitsyn, O. B., The molten globule state (1992) Protein Folding, pp. 243-300. , Creighton, T. E., ed. W. H. Freeman and Company, New York
Martin, J. L., Thioredoxin: A fold for all reasons (1995) Structure, 3, pp. 245-250. , Cambridge, MA, U. S. A
Kennedy, D. F., Crisma, M., Toniolo, C., Capman, D., Studies of peptides forming 310- and -helices and -bend ribbon structures in organic solutions and in model biomembranes by Furier transform infrared spectroscopy (1991) Biochemistry, 30, pp. 6541-6548
Bychkova, V. E., Dujsekina, A. E., Klenin, S. I., Tiktopulo, E. I., Uversky, V. N., Ptitsyn, O. B., Molten globule-like state of cytochrome c under conditions simulating those near the membrane surface (1996) Biochemistry, 35, pp. 6058-6063
Bychkova, V. E., Pain, R. H., Ptitsyn, O. B., The molten globule state is involved in the translocation of proteins across membranes? (1988) FEBS Lett., 238, pp. 231-234
Dolgikh, D. A., Gilmanshin, R. I., Brazhnikov, E. V., Bychkova, V. E., Semisotnov, G. V., Venyaminov, S. Yu., Ptitsyn, O. B., -lactalbumin: Compact state with fluctuating tertiary structure? (1981) FEBS Lett., 138, pp. 311-315
Dolgikh, D. A., Abaturov, L. V., Bolotina, I. A., Brazhnikov, E. V., Bushuev, V. N., Bychkova, V. E., Gilmanshin, R. I., Ptitsyn, O. B., Compact state of a protein molecule with pronounced small-scale mobility: Bovine -lactalbumin (1985) Eur. Biophys. J., 13, pp. 109-121
Structural and thermal stability analysis of Escherichia coli and Alicyclobacillus acidocaldarius thioredoxin revealed a molten globule-like state in thermal denaturation pathway of the proteins: an infrared spectroscopic study
The structure of thioredoxin from Alicyclobacillus acidocaldarius (previously named Bacillus acidocaldarius) (BacTrx) and from Escherichia coli (E. coli Trx) was studied by Fourier-transform IR spectroscopy. Two mutants of BacTrx [Lys(18) --> Gly (K18G) and Arg(82) --> Glu (R82E)] were also analysed. The data revealed similar secondary structures in all proteins, but BacTrx and its mutants showed a more compact structure than E. coli Trx. In BacTrx and its mutants, the compactness was p(2)H-dependent. All proteins revealed the existence of a molten globule-like state. At p(2)H 5.8, the temperature at which this state was detected was higher in BacTrx and decreased in the different proteins in the following order: BacTrx > R82E > K18G > E. coli Trx. At neutral or basic p(2) H, the molten globule-like state was detected at the same temperature in both BacTrx and R82E, whereas it was found at the same temperature in all p2 Hs tested for E. coli Trx. The thermal stability of the proteins was in the following order at all p2Hs tested: BacTrx > R82E > K18G > E. coli Trx, and was lower for each protein at p2H 8.4 than at neutral or acidic p2Hs. The formation of protein aggregates, brought about by thermal denaturation, were observed for BacTrx and K18G at all p2Hs tested, whereas they were present in R82E and E. coli Trx samples only at p2 H 5.8. The results indicated that a single mutation might affect the structural properties of a protein, including its propensity to aggregate at high temperatures. The data also indicated a possible application of Fourier-transform IR spectroscopy for assessing molten globule-like states in small proteins.
Structural and thermal stability analysis of Escherichia coli and Alicyclobacillus acidocaldarius thioredoxin revealed a molten globule-like state in thermal denaturation pathway of the proteins: an infrared spectroscopic study
Structural and thermal stability analysis of Escherichia coli and Alicyclobacillus acidocaldarius thioredoxin revealed a molten globule-like state in thermal denaturation pathway of the proteins: an infrared spectroscopic study